The global SARS-CoV-2 pandemic and the role of bats in zoonotic spillover have renewed interest in the flight-as-fever hypothesis, which posits that high body temperatures experienced by bats during flight contribute to their high viral tolerance. We argue that flight-as-fever is unlikely to explain why bats harbor more viruses than other mammals on the basis of two lines of reasoning. First, flight temperatures reported in the literature overestimate true flight temperatures because of methodologic limitations. Second, body temperatures in bats are only high relative to humans, and not relative to many other mammals. We provide examples of mammals from diverse habitats to show that temperatures in excess of 40 C during activity are quite common in species with lower viral diversity than bats. We caution scientists against stating the flight-as-fever hypothesis as unquestioned truth, as has repeatedly occurred in the popular media in the wake of the SARS-CoV-2 pandemic.

The recent emergence of SARS-CoV-2 and the associated global pandemic likely has its origins in wildlife, including possible bat reservoirs and unknown intermediate hosts (Andersen et al. 2020). This speculation has renewed discussion in both the scientific literature and, especially, the popular media about why bats can seemingly tolerate viruses that are lethal in spillover hosts such as humans. Bats are reservoir hosts of disproportionately more zoonotic pathogens than other groups (Luis et al. 2013; Olival et al. 2017). One hypothesis attempting to explain the high viral diversity in bats, the flight-as-fever hypothesis, has gained renewed attention as of late. The flight-as-fever hypothesis states that high metabolic rates and body temperatures associated with flight offer a level of protection to bats that differs from other mammals (O'Shea et al. 2014). The researchers who coined flight-as-fever posit that high body temperatures associated with flight (reported as high as 41–42 C) mimic fever, one of the most common mammalian responses to disease. Under these conditions, viruses in bats purportedly evolved the ability to withstand high body temperatures, rendering the febrile response in new hosts, such as humans and other terrestrial mammals, less effective in combating those viruses once contracted.

Although bats certainly harbor many zoonotic viruses (Luis et al. 2013; Olival et al. 2017), likely because they are one of the most species-rich mammalian orders (Mollentze and Streicker 2020), the hypothesis that high body temperature associated with flight relates to the virulence of bat-associated viruses is unlikely for several reasons. As has been argued convincingly elsewhere, the febrile response is only one of many immunologic responses, and flight would create no pressure for pathogens to evolve adaptations for dealing with the other defenses that are not induced by flight (Schountz et al. 2017). However, we presently have a limited understanding of bat immune responses (Schountz 2014; Schountz et al. 2017; Banerjee et al. 2020).

Our critique stems from the incorrect assumptions about thermoregulation in bats that form the basis of the flight-as-fever hypothesis. Nearly all evidence for an increase in body temperature during flight in bats comes from point measurements of rectal temperatures taken after capturing bats in the wild or after flights in a wind tunnel. Even ignoring the difficulties in describing body temperature of endothermic species with a single point measurement, this method is likely biased on the basis of simple biophysics. The heat produced by metabolic processes during flight is substantial but countered by radiative heat loss to the sky and convective heat loss to the quickly moving air around the body. Indeed, the wings remain cooler than the core during flight, and the large wing surface area provides a mechanism for heat dumping (Rummel et al. 2019). When captured, the decrease in metabolic rate is not instantaneous. Conversely, radiative heat loss to the sky will drop drastically and convective heat loss will instantly decrease to near zero as an animal is handled. The combination of a high metabolic rate and low heat loss likely drives the body temperature up briefly. Metabolic rate should decrease from the high levels necessary for powering flight to a lower maintenance level after capture, so you might also expect body temperature to decrease after a few minutes (Muise et al. 2018). Furthermore, the two most thorough studies reporting bat flight temperature provide little evidence to support the notion of large increases in body temperature during flight in bats. Barclay et al. (2017) implanted temperature-sensitive transmitters into Egyptian fruit bats and recorded body temperatures while the bats were in their roost. Although they did not measure body temperatures when bats were flying outside the roost, the body temperatures measured as bats returned to the roost after long foraging flights were rarely above 39 C. Likewise, Rummel et al. (2019) demonstrated that flight muscle temperature does not increase during flight in bats, often remaining below rectal temperature taken immediately after flying. In other words, many of the temperatures (up to 42 C) reported in the literature likely overestimate the true body temperature of bats during flight.

Even if we accept the high body temperatures during flight reported in the literature, it is a misunderstanding of mammalian thermoregulation to suggest these temperatures are unusually high for mammals. Over the last decade, increased work in desert, subtropical, and tropical regions has begun showing that many mammals regularly experience body temperatures at or above 40 C. Libyan jirds (Meriones libycus; Alagaili et al. 2017) and Arabian oryx (Oryx leucoryx) in Saudi Arabia (Hetem et al. 2010) reach body temperatures above 41 C regularly during summer and often above 39 C during winter (Fig. 1). Desert ground squirrels (Ammospermophilus leucurus; Chappell and Bartholomew 1981), tropical treeshrews (Tupaia tana; Levesque et al. 2018), and even the marsupial antechinus (Antechinus flavipes; Matthews et al. 2017) regularly reach 40 C, but none of these species are thought to carry the high viral loads found in bats. We have good-quality body temperature data representing only a tiny fraction of the diversity in mammals, and yet examples of species with high body temperatures are easy to find. Given the prevalence of such high body temperatures among the small number of species measured to date, body temperatures above 40 C during activity are obviously common in mammals. The paradigm of “normal” mammalian body temperatures hovering around 37 C stems from a time when nearly all relevant research was being conducted by North American and European researchers on temperate-zone species, where mammals rarely experience body temperatures above 38 C. However, even nocturnal southern flying squirrels (Glaucomys volans) from North America reach temperatures as high as 40.5 C during activity (Fig. 1). The high body temperatures reported for bats during flight are only outliers if the expected body temperature is that of humans.

Figure 1

Fluctuations in body temperature over 10-d periods for free-ranging (A) Libyan jird (Meriones libycus; Alagaili et al. 2017); (B) Arabian oryx (Oryx leucoryx; Hetem et al. 2010); (C) large treeshrew (Tupaia tana; Levesque et al. 2018); and (D) southern flying squirrel (Glaucomys volans, D.L.L. and V. Hensley pers. comm.). Traces were drawn from data provided by the authors. The dashed line represents the lower limit of febrile temperatures in mammals (O'Shea et al. 2014). Oscillations are due to the circadian rhythm.

Figure 1

Fluctuations in body temperature over 10-d periods for free-ranging (A) Libyan jird (Meriones libycus; Alagaili et al. 2017); (B) Arabian oryx (Oryx leucoryx; Hetem et al. 2010); (C) large treeshrew (Tupaia tana; Levesque et al. 2018); and (D) southern flying squirrel (Glaucomys volans, D.L.L. and V. Hensley pers. comm.). Traces were drawn from data provided by the authors. The dashed line represents the lower limit of febrile temperatures in mammals (O'Shea et al. 2014). Oscillations are due to the circadian rhythm.

Close modal

Taken together, the most parsimonious interpretation of the available data would suggest that 1) reported flight temperatures in bats are probably overestimated and, 2) even if reported body temperatures turn out to be correct, they are not strikingly high. There are two mutually exclusive conclusions relevant to the flight-as-fever hypothesis. If body temperature is the driving factor of high viral richness, then many tropical, subtropical, and desert mammals should also have high viral loads and be common sources for zoonotic diseases. This could be tested easily by studying the viral diversity of these species and other species known to have high body temperature. Conversely, and more likely, bats are not unique in terms of the active body temperatures they maintain, and the flight-as-fever hypothesis is incorrect. Clearly, proper measurements of flight temperatures in bats are needed. Although body size limitations currently exclude many small bats from such experiments, it is feasible to collect such data on larger bats, like the fruit bats commonly associated with zoonotic diseases. Until these data are collected, the current evidence aligns strongly against the untested flight-as-fever hypothesis, and we caution against the promotion of this hypothesis in both scientific and popular literature.

This work was supported by the US Department of Agriculture National Institute of Food and Agriculture, hatch project ME0-21911, through the Maine Agricultural and Forest Experiment Station. Maine Agricultural and Forest experiment publication 3748.

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